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Actin Depolymerization Is Sufficient to Induce Programmed Cell Death in Self-Incompatible Pollen

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Actin Depolymerization Is Sufficient to Induce Programmed Cell Death in Self-Incompatible Pollen JCB: ARTICLE Actin depolymerization is suffi cient to induce programmed cell death in self-incompatible pollen Steven G. Thomas,1 Shanjin Huang,2 Shutian Li,1 Christopher J. Staiger,2,3 and Vernonica E. Franklin-Tong1 1School of Biosciences, University of Birmingham, Edgbaston, Birmingham B15 2TT, England, UK 2Department of Biological Sciences and 3Bindley Bioscience Center, Purdue University, West Lafayette, IN 47907 elf-incompatibility (SI) prevents inbreeding through actin fi lament levels or dynamics play a functional role in specifi c recognition and rejection of incompatible initiating PCD in P. rhoeas pollen, triggering a caspase-3– pollen. In incompatible Papaver rhoeas pollen, SI like activity. Signifi cantly, SI-induced PCD in incompatible S 2+ triggers a Ca signaling cascade, resulting in the inhibi- pollen was alleviated by pretreatment with Jasp. This rep- tion of tip growth, actin depolymerization, and pro- resents the fi rst account of a specifi c causal link between grammed cell death (PCD). We investigated whether actin actin polymerization status and initiation of PCD in a plant dynamics were implicated in regulating PCD. Using the cell and signifi cantly advances our understanding of the actin-stabilizing and depolymerizing drugs jasplakinolide mechanisms involved in SI. Downloaded from (Jasp) and latrunculin B, we demonstrate that changes in www.jcb.org Introduction Self-incompatibility (SI) is one of the systems that prevent self- and Yao, 2004; van Doorn and Woltering, 2005) have been fertilization in fl owering plants. SI is controlled by a multiallelic documented. Features of PCD in animal cells include cyto- on July 17, 2006 S locus; S-specifi c pollen rejection results from the interaction chrome c leakage from the mitochondria, DNA fragmentation, of pollen S and pistil S determinants that have matching alleles and caspase activation. In animal cells, apoptosis is mediated (Franklin-Tong and Franklin, 2003). In Papaver rhoeas, the by a caspase cascade. Activated caspases cleave numerous sub- pistil S proteins (Foote et al., 1994) act as ligands, triggering strates, including endogenous nuclease inhibitors, resulting in 2+ increases in the cytosolic-free calcium concentration ([Ca ]i) the fragmentation of nuclear DNA. Although PCD should theo- in incompatible pollen (Franklin-Tong et al., 1993, 1997). The retically involve a caspase-3–like activity, no caspase homo- Ca2+-mediated signaling network results in the rapid inhibition logues have been found in plants (Woltering et al., 2002). of incompatible pollen tube growth. Within a few minutes of SI Despite this, there is good evidence for caspase-like activities signals, reorganization and massive, sustained depolymerization in plant cells (Lam et al., 2001; Schaller, 2004). We recently re- THE JOURNAL OF CELL BIOLOGY of the pollen fi lamentous actin (F-actin) is induced (Geitmann ported that SI triggers a PCD cascade in incompatible P. rhoeas et al., 2000; Snowman et al., 2002). Although the extent of F-actin pollen, which involves a caspase-3–like activity (Thomas and depolymerization during SI is clearly suffi cient to inhibit pollen Franklin-Tong, 2004). This provides a precise mechanism for tube growth, it appears to be a gross excess over the amount re- the specifi c destruction of incompatible pollen. quired to achieve this. This suggested possible additional func- As the actin cytoskeleton is a major target and effector of tions for the alteration to actin dynamics. signaling cascades in both animal and plant cells (Schmidt and Unwanted cells are usually removed by programmed cell Hall, 1998; Staiger, 2000), we explored a possible role for actin death (PCD). Many examples of PCD in plant development depolymerization in signaling to PCD. Recent evidence sug- (Kuriyama and Fukuda, 2002) and in responses to external gests that either stabilization or depolymerization of the actin stimuli (Swidzinski et al., 2002; Danon et al., 2004; Greenberg cytoskeleton is adequate to induce PCD in yeast and some animal cells, depending on the cell type (Levee et al., 1996; S.G. Thomas and S. Huang contributed equally to this paper. Janmey, 1998; Korichneva and Hammerling, 1999; Rao et al., Correspondence to Vernonica E. Franklin-Tong: [email protected] 1999; Morley et al., 2003; Gourlay et al., 2004; for review see Abbreviations used in this paper: CD, cytochalasin D; F-actin, fi lamentous actin; Gourlay and Ayscough, 2005). It is postulated that the alteration G-actin, globular actin; GM, germination medium; Jasp, jasplakinolide; LatB, latrunculin B; PCD, programmed cell death; ROS, reactive oxygen species; of actin fi lament dynamics initiates or modulates the apoptotic SI, self-incompatibility. signaling cascade (Janmey, 1998; Korichneva and Hammerling, © The Rockefeller University Press $8.00 The Journal of Cell Biology, Vol. 174, No. 2, July 17, 2006 221–229 http://www.jcb.org/cgi/doi/10.1083/jcb.200604011 JCB 221 1999; Rao et al., 1999; Morley et al., 2003; Gourlay et al., 2004), thereby committing cells to die (for review see Gourlay and Ayscough, 2005). Because PCD is triggered by SI in incom- patible P. rhoeas pollen (Thomas and Franklin-Tong, 2004), we hypothesized that early SI-induced actin depolymerization might play a role in acting as an upstream component in PCD activation. We have investigated this possibility using specifi c drugs to alter actin polymerization status in pollen tubes. Results Jasplakinolide stabilizes actin fi laments and alleviates SI-induced PCD Pollen tubes have a characteristic F-actin organization (Fig. 1 A), and SI induces the rapid depolymerization of actin fi laments and bundles (Fig. 1 B). To test the hypothesis that SI-stimulated PCD is triggered by actin depolymerization, we used jasplakino- lide (Jasp), which stabilizes actin fi laments and stimulates poly- merization (Bubb et al., 1994; Bubb et al., 2000) and has been shown to inhibit pollen tube growth (Cardenas et al., 2005). We found that 0.5 μM Jasp disrupted P. rhoeas pollen tube actin or- Downloaded from ganization, which induced actin fi lament bundling and aggregation (Fig. 1 C), and inhibited tip growth (unpublished data). The effect of Jasp on actin organization was essentially the opposite of that induced by SI. We examined whether transient treatments with Jasp might www.jcb.org “rescue” SI-induced pollen from PCD by counteracting the ac- Figure 1. Jasp alters actin organization and alleviates PCD induced by SI tin depolymerization. One of the hallmark features of PCD, in P. rhoeas pollen tubes. (A) Rhodamine-phalloidin staining shows normal DNA fragmentation, is triggered by SI and involves a caspase-3– organization of F-actin in an untreated P. rhoeas pollen tube. (B) Rhodamine- phalloidin staining shows major disruption of F-actin after 10 min of SI like activity (Thomas and Franklin-Tong, 2004). This was used induction. (C) Immunolocalization of actin alterations induced by 0.5 μM on July 17, 2006 as a marker for PCD and was assessed using TUNEL (Fig. 1, Jasp for 10 min shows dramatic rearrangement and stabilization of actin D and E). The induction of SI, which is caused by exposing fi laments. (D) DNA fragmentation, detected by TUNEL labeling, in a pollen tube treated with 1 μM LatB for 10 min. DAPI staining (right) shows that the incompatible pollen to S proteins for 30 min, produced high lev- TUNEL-positive signal (left) corresponds to nuclear DNA. (E) A typical con- els of DNA fragmentation of 55.2%, which was only slightly trol pollen tube shows no TUNEL-positive signal (left) corresponding to nu- lower than levels of 65.4% induced by SI for 8 h and signifi - clear DNA (right) despite overexposure revealing the background signal. < Bars, 10 μm. (F) Induction of SI for 30 min produced high levels of DNA cantly different from control levels of 16.8% (P 0.001; Fig. 1 F). fragmentation, which was only slightly lower than that achieved by an 8-h These data indicated that the interaction of incompatible pollen treatment (SI, 8 h). Consecutive (CON) treatment, in which 0.5 μM Jasp with S proteins for 30 min was suffi cient to trigger PCD. As we was added for 20 min to pollen tubes that had previously been treated for 10 min with S proteins, signifi cantly reduced the level of DNA fragmenta- had previously demonstrated that 10 min of SI stimulated a tion. Simultaneous (SIM) treatments of SI and Jasp for 30 min also signifi - 65% reduction in F-actin levels (Snowman et al., 2002), we al- cantly reduced levels of DNA fragmentation. Untreated pollen tubes lowed SI to progress for 10 min to ensure that a signifi cant level (control) produced low levels of DNA fragmentation, whereas 0.5 μM Jasp μ treatment for 30 min produced higher levels than controls but lower than of actin depolymerization had occurred and then added 0.5 M those induced by 30 min of SI. Values are mean percentages ± SEM (error Jasp for 20 min (see Pollen treatments). This consecutive treat- bars; n = 3). ment signifi cantly reduced DNA fragmentation (Fig. 1 F) by 32% (P = 0.04). Simultaneous treatment with SI and Jasp for 30 min also resulted in signifi cantly reduced levels of DNA To clarify whether actin depolymerization itself could induce fragmentation (33.8%; P < 0.001; Fig. 1 F). This demonstrates PCD, latrunculin B (LatB; Spector et al., 1983; Coue et al., that Jasp can alleviate SI-induced PCD. These data indicate that 1987) was used to depolymerize the actin cytoskeleton in grow- the actin depolymerization triggered by SI plays a functional ing P. rhoeas pollen tubes. LatB caused the rapid disruption role in the initiation phase of PCD in pollen tubes. of F-actin organization (Fig. 2, A and B) and the inhibition of pollen tube growth (unpublished data). To confi rm actin depoly- Latrunculin B reduces the level of F-actin merization, we measured F-actin levels (Gibbon et al., 1999; in P.
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